Oxidative ecology of paternal care in wild smallmouth bass, Micropterus dolomieu.

Physiologically, oxidative stress is considered a homeostatic imbalance between reactive oxygen species production and absorption. From an ecological perspective, oxidative stress may serve as an important constraint to life-history traits, such as lifespan, reproduction and the immune system, and is gaining interest as a potential mechanism underlying life-history trade-offs. Of late, there has been much interest in understanding the role of oxidative stress in the ecology of wild animals, particularly during challenging periods such as reproduction. Here, we used a long-term study population of a fish with sole-male parental care, the smallmouth bass, Micropterus dolomieu, to examine the associations among oxidative stress indicators and life-history variables in nest-guarding males. In addition, we investigated the potential role of oxidative stress as a physiological mediator of the life-history trade-off decision of paternal smallmouth bass to stay with or abandon their brood. We found that oxidative stress was significantly related to the life history of paternal smallmouth bass, such that older, larger fish with greater reproductive experience and larger broods nesting in cooler water temperatures had lower levels of oxidative stress. However, we found no significant correlation between oxidative stress and nesting success, suggesting that oxidative stress may not be involved in the decision of male smallmouth bass to abandon their brood. Wild fish have been relatively understudied in the emerging field of oxidative ecology, and this study makes noteworthy contributions by revealing interesting connections between the life histories of paternal smallmouth bass and their oxidative status.

Recreational fishing selectively captures individuals with the highest fitness potential.

Fisheries-induced evolution and its impact on the productivity of exploited fish stocks remains a highly contested research topic in applied fish evolution and fisheries science. Although many quantitative models assume that larger, more fecund fish are preferentially removed by fishing, there is no empirical evidence describing the relationship between vulnerability to capture and individual reproductive fitness in the wild. Using males from two lines of largemouth bass (Micropterus salmoides) selectively bred over three generations for either high (HV) or low (LV) vulnerability to angling as a model system, we show that the trait "vulnerability to angling" positively correlates with aggression, intensity of parental care, and reproductive fitness. The difference in reproductive fitness between HV and LV fish was particularly evident among larger males, which are also the preferred mating partners of females. Our study constitutes experimental evidence that recreational angling selectively captures individuals with the highest potential for reproductive fitness. Our study further suggests that selective removal of the fittest individuals likely occurs in many fisheries that target species engaged in parental care. As a result, depending on the ecological context, angling-induced selection may have negative consequences for recruitment within wild populations of largemouth bass and possibly other exploited species in which behavioral patterns that determine fitness, such as aggression or parental care, also affect their vulnerability to fishing gear.

Reproductive history and nest environment are correlated with circulating androgen and glucocorticoid concentrations in a parental care-providing teleost fish.

Using a long-term study population of wild smallmouth bass Micropterus dolomieu in a connected river-lake system, we investigated whether circulating glucocorticoid (cortisol) and androgen (testosterone) concentrations are influenced by reproductive investment and nesting environment in fish providing nest-guarding paternal care. For all individuals, we collected measures of reproductive history and the value of current parental care. We assessed nest environment and monitored individuals to quantify seasonal reproductive success. Finally, we measured circulating cortisol concentrations following a standardized stressor and circulating testosterone concentrations. Using general linear models, we found that poststress circulating cortisol concentrations were positively related to water temperature and were higher in fish nesting in the river than in the lake. Circulating testosterone concentrations were negatively related to water temperature and were higher in reproductively experienced fish. When considering the factors that influence reproductive success, we found that only parental size was positively related to current nest success. In summary, the results demonstrate that nesting environment is correlated with parental stress responses during parental care, while reproductive history and nesting environment are correlated with circulating androgen concentrations. Collectively, these results offer insight into the roles of both glucocorticoid and androgen steroid hormones during parental care in teleost fish.

The physiological response of the Caribbean reef shark (Carcharhinus perezi) to longline capture.

Longline fishing is the most common elasmobranch capture method around the world, yet the physiological consequences of this technique are poorly understood. To quantify the sub-lethal effects of longline capture in the commonly exploited Caribbean reef shark (Carcharhinus perezi), 37 individuals were captured using standard, mid-water longlines. Hook timers provided hooking duration to the nearest minute. Once sharks were landed, blood samples were taken and used to measure a suite of physiological parameters. Control data were obtained by sampling an additional three unrestrained Caribbean reef sharks underwater at an established shark feeding site. The greatest level of physiological disruption occurred after 120-180min of hooking, whereas sharks exposed to minimal and maximal hook durations exhibited the least disturbed blood chemistry. Significant relationships were established between hooking duration and blood pH, pCO(2), lactate, glucose, plasma calcium and plasma potassium. Longline capture appears more benign than other methods assessed to date, causing a shift in the stress response from acute at the onset of capture to a sub-acute regime as the capture event progresses, apparently facilitating a degree of physiological recovery. Continued investigation into the physiological response of elasmobranchs to longline capture is vital for the effective management of such fisheries.

Influence of behavior and mating success on brood-specific contribution to fish recruitment in ponds.

One source of uncertainty in predicting the response of populations to exploitation is individual differences within a population in both vulnerability to capture and contribution to population renewal. For species with parental care, individuals engaged in nesting behavior are often targeted for exploitation, but predicting outcomes of this nonrandom vulnerability will depend in part on an understanding of how parental traits are related to potential for brood contribution to the population. Variation in brood-specific contribution to recruitment of largemouth bass (Micropterus salmoides), a fish species with extended parental care, was quantified to determine if differences in mating success, parental care behaviors, and timing of reproduction influenced offspring recruitment. Dependence of these relationships on brood predation was tested in communities that differed in the presence of bluegill, Lepomis macrochirus, an important nest predator. Daily snorkel surveys were conducted in experimental ponds during spring to monitor male spawning and parental care behaviors in populations of largemouth bass. Tissue samples collected from larvae in nests were used to develop brood-specific DNA fingerprints for determining nest origins of fall recruits. Largemouth bass spawning period in bluegill ponds was longer and more variable in duration, with lower, more variable mating success, than in ponds without bluegill. In all populations, only one or two broods provided the majority of recruits, and these were broods produced during the earliest days of spawning by the oldest, largest males. In bluegill ponds, brood contribution from earliest nests also increased with brood size. Earliest nesters were the oldest males, and recruits from these nests were often above average in body size. Offspring needed to be guarded to at least swim-up larval stage to contribute any recruits. Termination of parental protection before offspring were free swimming mainly occurred with broods guarded by smaller males in ponds with brood predators. These age- and size-specific differences in timing of spawning and duration of parental care are consistent with influences of residual reproductive value and energetic constraints on reproductive behavior. Furthermore, these patterns of individual contribution to recruitment imply that fisheries that selectively target either nesting individuals or larger, older males could potentially decrease recruitment at the population scale.

Seasonal carryover effects following the administration of cortisol to a wild teleost fish.

Stress can have sublethal effects that are manifested either immediately or at spatial or temporal scales that are removed from the stress event (i.e., carryover effects). We tested whether a short-term elevation of plasma cortisol would result in seasonal carryover effects in wild largemouth bass Micropterus salmoides. Using exogenous hormone implants, we raised circulating cortisol concentrations in a group of wild fish for approximately 5 d in October 2007. We then compared activity (velocity, distance traveled) of cortisol-treated animals with that of sham-treated and control animals throughout the winter using an automated acoustic telemetry array. Immediately following treatment, the cortisol-treated fish showed increased activity relative to controls. However, this difference disappeared following the cessation of the elevation of circulating cortisol. During the winter of 2007 to 2008, the lake experienced a nearly complete winterkill event, providing insight into how a transient stress response can influence the response of wild animals to subsequent challenges. Most fish carrying acoustic transmitters succumbed during this winterkill event, but cortisol-treated fish died earlier than fish in other groups and showed a decrease in activity relative to controls and sham-treated fish before mortality. This study provides preliminary evidence of seasonal carryover effects in wild fish and yields insight into the ecological consequences of stress across broad temporal scales.

Cardiovascular performance of six species of field-acclimatized centrarchid sunfish during the parental care period.

Parental care is an energetically costly period of the life history of many fish species characterized by extended high intensity activity. To date, there have been no studies that have investigated the cardiovascular correlates of extended parental care in fish. Using Doppler flow probes, the cardiovascular performance of six syntopic centrarchid fish species (N=232) that provide sole, male parental care was examined across a range of water temperatures that encompass their reproductive periods (14-26 degrees C). Experiments were restricted to males but included both nesting and non-nesting individuals to evaluate the cardiovascular performance of fish during parental care. Resting values for cardiac output (Q) and heart rate (f(H)) tended to be higher for nesting fish when adjusted for variation in temperature. Both of these cardiac variables also increased with water temperature. Stroke volume (V(S)) was similar among nesting and non-nesting fish and was generally thermally insensitive. When exposed to exhaustive exercise, nesting fish took longer to exhaust than non-nesting individuals. The high resting levels found in nesting fish accompanied by only minor increases in maximal values typically resulted in reductions in cardiac scope. Cardiovascular variables recovered more quickly in nesting fish, which could facilitate the high activity and bursting associated with parental care. Interspecifically, several cardiovascular variables were correlated with parental care activity. Parental care investment became more energetically expensive as the degree of cardiac frequency modulation decreased. Additionally, as the duration of parental care increased, so did the time required for fish to become exhausted, although this relationship was probably influenced by the fact that the larger species (e.g. smallmouth bass Micropterus dolomieu; largemouth bass Micropterus salmoides) provided the lengthiest care. Collectively, these data indicate that fish that provide parental care possess adaptations, including sufficient phenotypic plasticity, such that they can enhance their ability to provide high intensity protracted care, and emphasize the nexus between behavior and physiology.

Effects of nutritional status on metabolic rate, exercise and recovery in a freshwater fish.

The influence of feeding on swimming performance and exercise recovery in fish is poorly understood. Examining swimming behavior and physiological status following periods of feeding and fasting is important because wild fish often face periods of starvation. In the current study, researchers force fed and fasted groups of largemouth bass (Micropterus salmoides) of similar sizes for a period of 16 days. Following this feeding and fasting period, fish were exercised for 60 s and monitored for swimming performance and physiological recovery. Resting metabolic rates were also determined. Fasted fish lost an average of 16 g (nearly 12%) of body mass, while force fed fish maintained body mass. Force fed fish swam 28% further and required nearly 14 s longer to tire during exercise. However, only some physiological conditions differed between feeding groups. Resting muscle glycogen concentrations was twofold greater in force fed fish, at rest and throughout recovery, although it decreased in both feeding treatments following exercise. Liver mass was nearly three times greater in force fed fish, and fasted fish had an average of 65% more cortisol throughout recovery. Similar recovery rates of most physiological responses were observed despite force fed fish having a metabolic rate 75% greater than fasted fish. Results are discussed as they relate to largemouth bass starvation in wild systems and how these physiological differences might be important in an evolutionary context.

Life-history traits and energetic status in relation to vulnerability to angling in an experimentally selected teleost fish.

In recreational fisheries, a correlation has been established between fishing-induced selection pressures and the metabolic traits of individual fish. This study used a population of largemouth bass (Micropterus salmoides) with lines of low vulnerability fish (LVF) and high vulnerability fish (HVF) that were previously established through artificial truncation selection experiments. The main objective was to evaluate if differential vulnerability to angling was correlated with growth, energetics and nutritional condition during the sub-adult stage. Absolute growth rate was found to be between 9% and 17% higher for LVF compared with HVF over a 6-month period in three experimental ponds. The gonadosomatic index in females was lower for LVF compared with HVF in one experimental pond. No significant differences in energy stores (measured using body constituent analysis) were observed between LVF and HVF. In addition, both groups were consuming the same prey items as evidenced by stomach content analysis. The inherent reasons behind differential vulnerability to angling are complex, and selection for these opposing phenotypes appears to select for differing growth rates, although the driving factors remain unclear. These traits are important from a life-history perspective, and alterations to their frequency as a result of fishing-induced selection could alter fish population structure. These findings further emphasize the need to incorporate evolutionary principles into fisheries management activities.

Physiological and behavioral consequences of long-term artificial selection for vulnerability to recreational angling in a teleost fish.

Few studies have examined the physiological and behavioral consequences of fisheries-induced selection. We evaluated how four generations of artificial truncation selection for vulnerability to recreational angling (i.e., stocks selected for high and low vulnerability [HVF and LVF, respectively]) affected cardiovascular physiology and parental care behavior in the teleost fish largemouth bass Micropterus salmoides. Where possible, we compared artificially selected fish to control fish (CF) collected from the wild. Although, compared to control fish, resting cardiac activity was approximately 18% lower for LVF and approximately 20% higher for HVF, maximal values did not vary among treatments. As a result, the HVF had less cardiac scope than either LVF or CF. Recovery rates after exercise were similar for HVF and CF but slower for LVF. When engaged in parental care activities, nesting male HVF were captured more easily than male LVF. During parental care, HVF also had higher turning rates and pectoral and caudal fin beat rates, increased vigilance against predators, and higher in situ swimming speeds. Energetics simulations indicated that to achieve the same level of growth, the disparity in metabolic rates would require HVF to consume approximately 40% more food than LVF. Selection for angling vulnerability resulted in clear differences in physiological and energetic attributes. Not only is vulnerability to angling a heritable trait, but high vulnerability covaries with factors including higher metabolic rates, reduced metabolic scope, and increased parental care activity. Despite these energetically costly differences, HVF and LVF of the same age were of similar size, suggesting that heightened food consumption in HVF compensated for added costs in experimental ponds. Ultimately, angling vulnerability appears to be a complex interaction of numerous factors leading to selection for very different phenotypes. If HVF are selectively harvested from a population, the remaining fish in that population may be less effective in providing parental care, potentially reducing reproductive output. The strong angling pressure in many freshwater systems, and therefore the potential for this to occur in the wild, necessitate management approaches that recognize the potential evolutionary consequences of angling.

Energetics of parental care in six syntopic centrarchid fishes.

We studied parental behavior in six syntopically breeding species of centrarchid fishes to determine whether energetic costs could contribute to our understanding of the diversity of parental care. We used a combination of underwater videography, radio telemetry and direct observation to examine how the cost of parental care varied with both its duration and intensity. Duration of parental care, activity patterns, and energetic costs varied widely among species. Overall, the duration of care increased with parental size between species. When energetic costs were adjusted for species-specific differences in the duration of parental care, the cost of parental care also increased with mean size of the species. Species with extended parental care exhibited stage-specific patterns of activity and energy expenditure consistent with parental investment theory, whereas fish with short duration parental care tended to maintain high levels of activity throughout the entire period of parental care. The only apparent exception (a species with brief parental care but stage-specific behavior) was a species with multiple breeding bouts, and thus effectively having protracted parental care. These data suggest that some species with short duration parental care can afford not to adjust parental investment over stages of offspring development. Using our empirical data on parental care duration and costs, we reevaluated the relationship between egg size and quality of parental care. Variation in egg size explained almost all of the observed variation in total energetic cost of parental care, and to a lesser degree, duration-the larger the eggs, the more costly the parental care. This research highlights the value of incorporating energetic information into the study of parental care behavior and testing of ecological theory.

Sex-specific life history patterns in bluegill (Lepomis macrochirus): interacting mechanisms influence individual body size.

The ultimate body size that an individual fish achieves can be a function both of direct effects of growth or indirect effects associated with the timing of sexual maturation (and associated energetic tradeoffs). These alternatives are often invoked to explain variation in body size within and among fish populations, but have rarely been considered simultaneously. We assessed how resource availability and timing of maturation interact to influence individual body size of bluegill (Lepomis macrochirus). Resource availability (high and low food) and the social structure of the population (presence or absence of large, mature males) were varied in experimental ponds. Food ration affected growth (larger fish in the high food treatments) and the social structure of the population affected timing of maturation (early maturation of males in the absence of large males). Treatment effects, however, were sex-specific; males responded to the social structure of the population and females were more responsive to resource availability. We also found individuals that became sexually mature were smaller than those that remained immature, although results were sex-specific and resource dependent. For males, individuals that matured were smaller when resources were limited; mature and immature females showed no difference in body size regardless of food ration. We show that both resource availability and the processes that control timing of maturation interact in sex-specific ways to influence body size of bluegill. These results suggest that a more robust explanation for variable body size requires consideration of sex-specific interactions between ecological (food and growth) and evolutionary (timing of maturation) mechanisms.

Influence of local adaptation and interstock hybridization on the cardiovascular performance of largemouth bass Micropterus salmoides.

In this study, the cardiovascular response to exhaustive exercise among differentiated stocks of largemouth bass Micropterus salmoides was compared at 10 degrees C and 20 degrees C to assess the level of their local adaptation. In addition, the impact that interstock hybridization had on adaptive differences was assessed using F1 hybrids. To accomplish these assessments, four genetically distinct stocks of fish were produced using adults from two regions in the midwestern United States identified as distinct conservation management units (central Illinois, IL and southeastern Wisconsin, WI): both P1 stocks and both reciprocal F1 interstock hybrids. Cardiac variables (both resting and maximal) were consistently lowest for the IL x IL stock relative to the WI x WI stock and both F1 interstock hybrids. Interestingly, however, all groups of fish were able to maintain similar levels of cardiac scope. All fish responded to exercise by increasing heart rate and decreasing stroke volume, consistent with the notion that largemouth bass modulate cardiac output via frequency. After exercise, cardiac variables returned to resting levels 25-35% more rapidly for IL x IL fish relative to all other groups at 20 degrees C. At 10 degrees C, recovery rates for both P1 stocks were similar but more rapid than the interstock hybrids. Collectively, these results indicate that the locally adapted stock (IL x IL) exhibited cardiovascular adaptations that enabled rapid cardiovascular recovery and maintenance of low resting cardiac output and heart rate. Conversely, the translocated stock (WI x WI) and the interstock hybrids required longer for cardiovascular variables to recover after exercise and exhibited higher resting levels of cardiac output and heart rate. This study provides some of the first direct evidence of a physiological mechanism by which mixing stocks could potentially decrease fitness and illustrates the magnitude of the intraspecific diversity of cardiovascular performance.

Effects of incremental increases in silt load on the cardiovascular performance of riverine and lacustrine rock bass, Ambloplites rupestris.

Rock bass (Ambloplites rupestris) are a widespread centrarchid species with both riverine and lacustrine populations. After precipitation events, rivers often carry elevated silt loads, where as lakes generally remain free from suspended silt and sediment. To examine the physiological effects of silt on rock bass, we conducted a series of experiments using fish from Lake Opinicon and the Grand River in Ontario. Ultrasonic Doppler flow probes were surgically affixed around the ventral aorta to monitor cardiovascular performance. After recovery from surgery replicated treatment groups were exposed to incremental increases in silt load (made from bentonite slurry), while cardiac output and its two components, heart rate and stroke volume, were measured simultaneously. Although both groups of rock bass responded significantly to low concentrations of silt (10 NTU), the response by riverine rock bass was rapidly extinguished by acclimation or physiological adjustment. Compensatory mechanisms to minimize cardiac (and respiratory) disruption attributable to increases in suspended silt appear to be inherent in rock bass of riverine origin. These fish appear to fully compensate for interference in gas exchange at the gill surfaces 60 min after initial exposure. In contrast, individual lacustrine rock bass were highly variable in their response to elevated silt concentrations. Changes in stroke volume and cardiac output suggested no clear compensatory mechanism or strategy to cope with increased silt levels.

Speciation in North American black basses, Micropterus (Actinopterygii: Centrarchidae).

The Pleistocene Epoch has been frequently cited as a period of intense speciation for a significant portion of temperate continental biotas. To critically assess the role of Pleistocene glaciations on the evolution of the freshwater fish clade Micropterus, we use a phylogenetic analysis of complete gene sequences from two mitochondrial genes (cytochrome b and ND2), and a fossil calibration of the molecular clock to estimate ages of speciation events and rates of diversification. The absence of substantial morphological and ecological divergence together with endemism of five of the eight species in North American tributaries of the Gulf of Mexico may be interpreted as the result of a recent Pleistocene origin for these species. Speciation dates in Micropterus range from 1.01 +/- 0.32 to 11.17 +/- 1.02 million years ago. Only one speciation event is dated to the Pleistocene, and rates of diversification are not significantly variable in Micropterus. The premise that the Pleistocene was an exceptional period of speciation in Micropterus is not supported. Instead, a Gulf Coast allopatric speciation model is proposed, and predicts periods of dynamic speciation driven by sea level fluctuations in the Late Miocene and Pliocene. The Pleistocene, however, was a period of significant intraspecific mitochondrial lineage diversification. The application of the Gulf Coast allopatric speciation model to the remaining aquatic fauna of the Gulf of Mexico coast in North America will rely on robust phylogenetic hypotheses and accurate age estimations of speciation events.

Strain variation in an emerging iridovirus of warm-water fishes.

Although iridoviruses vary widely within and among genera with respect to their host range and virulence, variation within iridovirus species has been less extensively characterized. This study explores the nature and extent of intraspecific variation within an emerging iridovirus of North American warm-water fishes, largemouth bass virus (LMBV). Three LMBV isolates recovered from three distinct sources differed genetically and phenotypically. Genetically, the isolates differed in the banding patterns generated from amplified fragment length polymorphism analysis but not in their DNA sequences at two loci of different degrees of evolutionary stability. In vitro, the isolates replicated at identical rates in cell culture, as determined by real-time quantitative PCR of viral particles released into suspension. In vivo, the isolates varied over fivefold in virulence, as measured by the rate at which they induced mortality in juvenile largemouth bass. This variation was reflected in the viral loads of exposed fish, measured using real-time quantitative PCR; the most virulent viral strain also replicated to the highest level in fish. Together, these results justify the designation of these isolates as different strains of LMBV. Strain variation in iridoviruses could help explain why animal populations naturally infected with iridovirus pathogens vary so extensively in their clinical responses to infection. The results of this study are especially relevant to emerging iridoviruses of aquaculture systems and wildlife.

Low temperature cardiac response to exhaustive exercise in fish with different levels of winter quiescence.

We examined the cardiac responses of different fish species to anaerobic exercise at low temperatures (3 degrees C). Three species of sympatric warmwater fish with perceived differences in winter activity were used for this comparative study: the winter-quiescent largemouth bass (Micropterus salmoides); the winter-active white bass (Morone chrysops); and the intermediately winter-active black crappie (Pomoxis nigromaculatus). Perceived differences in winter activity were reflected in cardiac responses; e.g. basal cardiac values were lowest for largemouth bass, highest for white bass, and intermediate for black crappie. In addition, cardiac recovery was most rapid for white bass, slowest for largemouth bass and intermediate for black crappie. When disturbed at low temperatures, largemouth bass and black crappie elevated cardiac output principally through increases in heart rate despite substantial decreases in stroke volume. Conversely, white bass principally used stroke volume modulation to change cardiac output. The results of this study indicate that different species respond differently to exercise at low temperatures. Management strategies should recognize that such variation exists and ensure that management decisions are based upon an understanding of the low temperature exercise physiology and winter biology of the species of interest.